Sex determination in zebrafish is not well understood. In AB and TU laboratory strains, sex determination occurs in the absence of a typical sex chromosome, but animals directly from nature have a strong sex determinant on LG4. Early stage oocytes are necessary for primary female sex determination, and therefore it is hypothesized that oocytes produce a signal that act on the somatic gonad that maintains female sex or inhibits male sex differentiation. In mammals, Wnt4 is a signaling ligand that is essential for female development. We therefore asked if wnt4a, the single copy ortholog of WNT4 in zebrafish, has a similar role in zebrafish primary sex determination. We found, using qPCR and in situ hybridization, that wnt4a is expressed in the somatic cells of juvenile gonads by 12 days post fertilization and continues in the follicle cells of adult ovaries. Thus wnt4a is a plausible candidate for the oocyte-produced sex determining factor. Fish homozygous for wnt4a(fh295), a TILLING allele that encodes a C-terminally truncated protein lacking residues shown to be important in WNT signaling, develop almost exclusively as male. Because the existing wnt4a TILLING alleles are C-terminal truncations and are therefore suspected dominant-negatives, we used CRISPR/Cas9 to produce two loss-of-function mutant alleles, wnt4a(uc55) and wnt4a(uc56), which result from a 17 and a 26 base pair insertion where in the protein is truncated to 68 or 33 amino acids, respectively. We found that homozygous adult mutants for both wnt4a(uc55) and wnt4a(uc56) develop predominantly as males. We further found that mutant males are sterile because reproductive ducts do not grow as rapidly toward the vent as wild-type ducts, and never connect to the genital orifice. However, sperm from macerated testes of wnt4a mutants produced normal offspring. Tissue surrounding the genital orifice in wild types strongly expressed wnt4a. These results show that Wnt4 is necessary for normal male reproductive duct development, but not for male sex determination. To further define the role of WNT signaling for female development and male duct development, we created CRISPR/Cas9 mutants in rspo1, which encodes a component of the canonical WNT signaling pathway. Our results strongly support the hypothesis that Wnt4a plays an important role in female sex determination and male reproductive duct development.